High prevalence of Ancylostoma spp. infection in dogs, associated

Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/1996032131
H ig h p r e v a l e n c e o f A n c y l o s t o m a s p p . in f e c t io n in d o g s ,
ASSOCIATED WITH ENDEMIC FOCUS OF HUMAN CUTANEOUS
LARVA MIGRANS, IN TACUAREMBO, URUGUAY
M A LG O R R.*, O K U Y .**, GALLARDO R.* & YA RZÁBAL L.*
Summary :
R ésu m é
A helminthological survey of the intestinal parasites in stray dogs
w as conducted in urban and suburban area of Tacuarembó,
Uruguay, during winter time. Eighty stray dogs captured in the city
were necropsied. Seventy nine dogs (9 8 .8 %) were positive for
helminth infection. Seventy seven (9 6 .3 %) were parasitized by
hookworms. Two species of hookworms were found: Ancylostoma
caninum 9 6 .3 % and A. braziliense 4 9 .4 %. This is the first report
of the prevalence of A . braziliense in Uruguay. Considering that
incidences of human cutaneous larva migrans caused by the
migration of hookworms larvae were restricted mainly to the
northen part of Uruguay and that only A . caninum were reported
to be prevalent in the southen part, it is supposed that A.
braziliense is the primary causative agent of human cutaneous
larva migrans in Uruguay.
KEYWORDS: helminth, nematoda, dog, Ancylostoma, prevalence, cutaneous
larva migrans, Uruguay.
: F o r te prévalence d e l ' in fection canine à ancylostoma
SPP. ASSOCIÉE À UN FOYER ENDÉMIQUE HUMAIN DE LARVA MIGRANS
CUTANÉE À TACUAREMBO, URUGUAY
Une étude helminthologique concernant les parasites intestinaux
chez des chiens vagabonds a été réalisée pendant l'hiver, dans
les quartiers urbains et suburbains de la ville de Tacuarembó en
Uruguay. Parmi les chiens capturés, quatre-vingts ont été autopsiés.
Soixante dix-neuf chiens (9 8 ,8 %) ont présenté une infection par
helminthes. Soixante dix-sept (9 6 ,3 %) étaient parasités par des
ankylostomes. Deux espèces de ce genre ont été trouvées :
Ancylostoma caninum 9 6 ,3 % et A. braziliense 4 9 ,4 %. C e
travail constitue le premier rapport de prévalence de
A. braziliense en Uruguay. En considérant que l'incidence
humaine de larva migrans cutanée, causée par la migration de
larves d'ancylostom atidés, se limite surtout à la région nord du
pays, et que seulement A. caninum a été rapporté dans la région
sud du pays, nous supposons que A. braziliense est le principal
agent étiologique de la larva migrans cutanée en Uruguay.
MOTS CLÉS : helminthe, nématode, chien, Ancylostoma, pré valence, larva
migrans cutanée, Uruguay.
IN TR O D U C TIO N
T
he zoonosis caused by canine parasites are an
interesting subject to study because o f the close
relationship betw een humans and dogs (Elliot
et al., 1985).
Uruguay is an endem ic country o f hydatidosis/echin o co cc o sis, o n e o f the m ost im portant zoon osis,
caused by E c h in o c o c c u s g ra n u losu s, and the disease
is usually related with rural areas, w here the cycle o f
the parasite is easily maintained (Purriel et al., 1973).
Numerous w ork has been carried out on hydatidosis
in Uruguay, however, other important zoonosis caused
by canine parasites w ere not studied adequately.
The disease called « creeping eruption », « cutaneous
larva migrans » or « sandworm » is caused by the infec­
tive larvae (L3) o f hookw orm s w ich penetrate the
* Unidad de Biología Parasitaria, Instituto de Higiene, Universidad
de la República Oriental del Uruguay, Avda. Alfredo Navarro 3051,
CP 11600, Montevideo, Uruguay. Fax : 598-2-473074.
** Department o f Animal Disease Control, Graduate School o f Vete­
rinary Medicine, Hokkaido University, Sapporo 060 Japan. Fax : 011709-1593.
Correspondence : Ramiro Malgor.
Parasite, 1996, 3, 131-134
unbroken skin o f man and migrate through subcuta­
neous tissue. As humans are not adequate hosts they
are unable to com plete their migratory cycle and pro­
duce skin lesions. The principal hookw orm s causing
cutaneous larva migrans are A n cy lostom a b raz ilien se,
U n c in a ria s t e n o c e p b a la , and B u n o s to m u m p h le b o tom u m , while A n c y lo sto m a c a n in u m plays only a
minor role (Soulsby, 1987). These agents are cosm o­
politan in temperate and tropical areas. Human infec­
tion usually occurs in areas w here recreational exp o­
sure to contaminated soil takes place, such as sandy
beach es or parks.
Ferreira and Ferreira (1991) reported 89 human cases
o f cutaneous larva migrans in Tacuarem bó from 1968
to 1989. All patients w ere residents o f urban and sub­
urban areas and the incidence was highest in summer
and beginning o f autumn. Ninety percent o f cases were
in the age group o f 1 to 10 years old.
In Montevideo, because o f the high num ber o f stray
dogs and the behavior o f dog owners that allow their
animals to defecate anywhere and leaves their feces
behind, contamination with hookworm eggs was reco­
gnized in many parks and public places (Perez, 1991).
Mémoire
131
:MALGOR "1¡
OKI
GALLARDO K. ¿i VAR/.ÁH \l. I..
However, the incidence o f cutaneous larva migrans is
very low.
This study was conducted to investigate the prevalence
o f gastro-intestinal helm inths o f dogs with special
emphasis on the prevalence o f A. b r a z ilie n s e as the
causative agent o f human cutaneous larva migrans.
MATERIALS A N D M ETHO DS
Parasite
Echinococcus granulosus
Taenia sp.
Multiceps sp.
Dipylidium caninum
Toxocara canis
Ancylostoma caninum
Ancylostoma braziliense
N° of dogs
3
6
1
30
%
3.8
7.5
1.3
37.5
8
10.0
77
38
96.3
49.4
Table I. - Prevalence o f parasites in dogs in Tacuarembó-Uruguay
T
he survey was carried out in Tacuarem bó, a
small city located in the north o f Uruguay at
31°42'7 South latitude and 55°59'5 W est longi­
tude and at 134.03 meters above sea level. It has
40,000 inhabitants, with an average annual rain preci­
pitate o f 1,100-1,200 mm, and an average annual tem ­
perature o f 17-18 °C. T he average tem perature in
summer during the last four years was 22.5 °C (range
6 °C to 38.5 °C) and in winter was 12 °C (range - 6 °C
to 30 °C). The rain precipitation in summer in the last
5 years was 400 to 500 mm annually.
From Ju n e to Septem ber 1992, 80 stray dogs (51 male
and 28 fem ale) captured for the Control Program on
Hydatid Disease in Tacuarem bó w ere necropsied. The
animals cam e from urban and sub-urban areas o f the
city. The small intestine o f each dog was removed and
divided into 3 equal parts in length, slit longitudinally
and the m ucosae scraped. To avoid biohazardous
risks, the contents w ere heated in a boiling waterbath.
The material was rinsed with tap water through a sieve
mesh (aperture 150 μ) and the retained on the mesh
was collected and sedimented.
The parasites w ere collected from the sedimentation
and fixed in 10 % formalin. All the hookw orm s were
transparenced with lactophenol and identified under
m icroscope, by the characteristics o f their buccal cap ­
sules (Matsusaki et a l., 1965; Yoshida, 1971; Yoshida
et a l., 1974).
Fig. 1. - Frequency distribution o f A. caninum .
Fig. 2. - Frequency distribution o f A. braziliense.
RESULTS
The m ean intensity o f infection was 57.5 (range 1-246)
for A. c a n in u m and 6.7 (range 1-57) for A. b raz ilien se.
T
No correlation was found betw een sex o f host and
worm burden.
he prevalence o f helminth infections is shown
in Table I. Seventy nine o f the dogs (98.8 %)
w ere positive for helminth infections. Seventy
seven o f the dogs (96.3 %) harboured hookworms.
Tw o species w ere identified: A n cy lostom a c a n in u m
and A. b r a z ilie n s e . All in fecte d dogs h arb o u red
A. c a n in u m while 49.4 % o f them harboured A. b r a ­
z ilien se. The most com m on species coinfected were
A n c y lo s to m a c a n in u m -A . b r a z ilie n s e , follow ed by
A. c a n in u m -D ip y llid iu m ca n in u m .
The male/female ratio o f parasite recovered was 0.6/1
and 0.5/1 for A. c a n in u m and A. b ra z ilien se, respec­
tively.
Figures 1 and 2 show the frequency distributions of
worm burden in each species o f A n cylostom a.
The distribution in the small intestine for A. c a n in u m
was: 44 % in the anterior, 45 % in the middle and 11 %
132
The distribution o f worm burden in A. c a n in u m was
found to be hyper-dispersed; only 6.5 % o f the dogs
had more than 200 parasites and the majority had less
than 100 with 45.5 % o f the dogs harboring betw een
10 and 50 parasites.
Mémoire
Parasite, 1996, 3, 131-134
A.VCYLOSTOMA SPP. ,N DOCS AND HUMAN CUTANEOUS LARVAE MIGRANS
in the posterior part; whereas A. b ra z ilie n se was: 69 %,
25 % and 6 %, respectively. The preference for the
anterior intestine is more evident in A. b raz ilien se.
DISCU SSIO N_______________________________
I
n this study, 7 species o f helminths w ere found in
dogs in Tacuarem bó. Even though the dogs were
cap tu red in urban and su bu rban area, sm all
num ber o f dogs w ere infected with E. g ran u losu s. This
finding presents an important implication in epide­
miology o f the disease that the hydatidosis is not only
a rural problem. The source o f E. g ra n u lo s u s found in
the dogs was not clear, however, it may be related to
the existance o f small illegal slaughterhouses around
the city.
More significantly, high prevalence o f A n cy lostom a
spp. was revealed in stray dogs in Tacuarem bó in this
study.
Table II shows the prevalence o f A n cy lostom a sp. in
dogs, reported in different countries. Although methods
with different sensitivity w ere used, the prevalence o f
A n cy lostom a sp. found in Tacuarem bó, Uruguay, was
ranked as the highest, suggesting that the environment
of Tacuarembó is suitable for the transmission o f A n cy­
lo sto m a sp.
The survey was carried out in winter w hen the mean
temperature in Tacuarem bó is 12 °C and sometimes
reaches under 0 °C. B ecause the developm ent o f eggs
to larva (L3) is restricted at cold temperature (Soulsby,
1987), the transmission o f hookw orm s is supposed to
b e low in winter.
It was reported that the prevalence rates varied with
the season and increased in the warm seasons (Mitra
et al., 1990). Therefore, it is indicated that the trans­
mission o f hookw orm s is higher in summer in Tacua­
rem bó and the rate o f infection or worm burden is also
higher. Supporting this, all human cases o f cutaneous
larva migrans reported in Tacuarem bó by Ferreira and
Ferreira (1991) w ere found in summer and at the begining o f autumm, w hen the skin is more exposed and
the num ber o f infective larvae in the environment is
higher. Cutaneous larva migrans w ere also found in
Salto, located in the north part o f Uruguay, and
Drs. Suarez and Calegari found 17 cases in summer
from D ecem ber 1982 to May 1983 (personal com m u­
nication).
In the south o f the country, how ever, cutaneous larva
migrans are not com m on. A study carried out in Mon­
tevideo, the capital of Uruguay and located in the south
o f the country, show ed that the prevalence o f hook­
worm o f 60 stray dogs exam ined was high (38 %) but
A. c a n in u m was the only species found (Dr. P. Ca­
brera, 1987). A b r a z ilie n s e which causes human cuta­
neous larva migrans has not been found in M onte­
Parasite, 1996, 3, 131-134
video. Most hum an cases reported in M ontevideo,
ocurred in patients infected during holiday time in
Brazil.
Because A. b r a z ilie n s e needs higher temperature to
successfully develop and com plete its cycle, compared
to A. c a n in u m , it is supposed that A. b r a z ilie n s e can
not maintain its life cycle in colder south region o f Uru­
guay such as M ontevideo. Considering that cutaneous
larva migrans w ere found only in the north region
w here A. b ra z ilie n se was prevalent, it is supposed that
the causative agent o f cutaneous larva migrans in Uru­
guay is mainly A. b raz ilien se.
Further studies are necessary to know what ecological
factors make Tacuarem bó and probably other cities in
the north o f the country a good environment for the
transmission o f A. b raz ilien se. It is also necessary to
study the prevalence o f A. b r a z ilie n s e in cats, another
suceptible host for this parasite for understanding the
role o f cat in this zoonosis.
High prevalence o f A. b r a z ilie n s e shown by this study
points out the importance o f this parasite in Uruguay
as the cause o f human illness. Although the prevalence
o f A. c a n in u m was very high, human cases o f eosi­
nophilic enteritis has not b een reported in Uruguay.
As Olivera et al. (1990) reported that improvement o f
sanitary conditions and education o f dog owners have
reduced the prevalence o f A n cy lostom a sp. in dogs in
Brazil, it is necessary in Uruguay to introduce some
regulations for regular treatment o f pets and to change
the behaviour o f people to prevent potentially more
severe outbreak o f the zoonosis.
Athens
(Georgia)
Japan (Shiga)
Spain (Galicia)
Jamaica
Australia
(Queensland)
Nigeria
(Calabar)
India
Brazil
(Sao Paulo)
Brazil
(Minas Gerais)
Uruguay
(Montevideo)
Uruguay
(Tacuarem bó)
Prevalence %
Year
Mean
intensity
86.0 A.c.
1951
141
18.6
24.6
22.7
20.1
A.sp
A.sp
A.sp
A.sp
Method
N
(5)
1984
1987
1986
1987
N
E
E
E
(16)
(2)
(14)
(4)
26.8 A.sp
1984
E
(17)
26.6 A.sp
59.8 A.sp
1988
1980-85
E
E
(10)
(1)
61.2 A.sp
1981-86
E
(11)
38.0 A.c.
1987
N
(3)
96.3 A.c.
49.4 A.b.
1992
57.5
6.7
N
A.c. A. ca n in u m ; A.b. A. braz ilien se; A. s.p. Ancylostom a s p .;
N: necrop sy ; E: egg exam ination.
Table II. - Prevalence of Ancylostomiasis in dogs in different coun­
tries.
133
MALGOR R., OKU Y., GALLARDO R. & YARZABAL L,
morbidity and mortality. Bulletin o f the Wold Health Orga­
nization, 1973, 49, 395-402.
ACKNOWLEDGEMENTS
T
his work was suported by JICA, Jap an Interna­
tional C ooperatioon Agency and Ministry o f
Education Science and Culture, Japan (grant
n° 06041005).
W e are grateful for the collaboration o f the Municipal
Governm ent o f Tacuarem bó.
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T ad a
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Parasite, 1996, 3, 131-134